Comparison of morphometric patterns and blood biochemistry in capybaras (Hydrochoerus hydrochaeris) of human-modified landscapes and natural landscapes

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(1)HECTOR RIBEIRO BENATTI. Comparison of morphometric patterns and blood biochemistry in capybaras (Hydrochoerus hydrochaeris) of human-modified landscapes and natural landscapes. São Paulo 2020.

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(3) HECTOR RIBEIRO BENATTI. Comparison of morphometric patterns and blood biochemistry in capybaras (Hydrochoerus hydrochaeris) of human-modified landscapes and natural landscapes. Thesis submitted to the Postgraduate Program in Experimental Epidemiology Applied to Zoonoses of the School of Veterinary Medicine and Animal Science of the University of São Paulo to obtain the Doctor’s degree in Sciences. Department: Preventive Veterinary Medicine and Animal Health Concentration area: Experimental Epidemiology Zoonoses. Applied. Advisor: Professor Marcelo Bahia Labruna, Ph.D.. According: ___________________________ Marcelo B. Labruna, Ph.D.. São Paulo 2020 Obs: A versão original encontra-se disponível na Biblioteca da FMVZ/USP.. to.

(4) Total or partial reproduction of this work is permitted for academic purposes with the proper attribution of authorship and ownership of the rights.. DADOS INTERNACIONAIS DE CATALOGAÇÃO NA PUBLICAÇÃO (Biblioteca Virginie Buff D’Ápice da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo). T. 3944 FMVZ. Benatti, Hector Ribeiro Comparison of morphometric patterns and blood biochemistry in capybaras (Hydrochoerus hydrochaeris) of human-modified landscapes and natural landscapes / Hector Ribeiro Benatti. – 2020. 90 f. : il. Título traduzido: Comparativo de padrões morfométricos e bioquímica do sangue de capivaras (Hydrochoerus hydrochaeris) de áreas antropizadas e áreas naturais. Tese (Doutorado) – Universidade de São Paulo. Faculdade de Medicina Veterinária e Zootecnia. Departamento de Medicina Veterinária Preventiva e Saúde Animal, São Paulo, 2020. Programa de Pós-Graduação: Epidemiologia Experimental Aplicada às Zoonoses. Área de concentração: Epidemiologia Experimental Aplicada às Zoonoses. Orientador: Prof. Dr. Marcelo Bahia Labruna. 1. Capivara. 2. Paisagens modificadas pelo homem. 3. Paisagens naturais. 4. Padrão morfométrico. 5. Perfil bioquímico. I. Título.. Ficha catalográfica elaborada pela bibliotecária Maria Aparecida Laet, CRB 5673-8, da FMVZ/USP..

(5) São Paulo, 18 de março de 2020 CEUA N 2308290917 IImo(a). Sr(a). Responsável: Marcelo Bahia Labruna Área: Medicina Veterinária Preventiva E Saúde Animal Título da proposta: "Comparativo de padrões morfométricos e bioquímica do sangue de capivaras (Hydrochoerus hydrochaeris) de áreas antropizadas e áreas naturais.". Parecer Consubstanciado da Comissão de Ética no Uso de Animais FMVZ (ID 005948) A Comissão de Ética no Uso de Animais da Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo, no cumprimento das suas atribuições, analisou e APROVOU a Alteração do cadastro (versão de 19/fevereiro/2020) da proposta acima referenciada. Resumo apresentado pelo pesquisador: "Solicita-se alteração apenas do Título,por recomendação da Banca de Qualificação. Nada mais mudou no projeto, que já encontra-se finalizado. A Tese será defendida daqui 2 meses, quando então, faremos a submissão como relatório Final. . ". Comentário da CEUA: "aprovado.".. Prof. Dr. Marcelo Bahia Labruna Coordenador da Comissão de Ética no Uso de Animais Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo. Camilla Mota Mendes Vice-Coordenador Faculdade de Medicina Veterinária e Zootecnia da Universidade de São Paulo. Av. Prof. Dr. Orlando Marques de Paiva, 87, Cidade Universitária: Armando de Salles Oliveira CEP 05508-270 São Paulo/SP - Brasil - tel: 55 (11) 3091-7676 Horário de atendimento: 2ª a 5ª das 7h30 às 16h : e-mail: ceuavet@usp.br CEUA N 2308290917.

(6) EVALUATION FORM. Author: BENATTI, Hector Ribeiro. Title: Comparison of morphometric patterns and blood biochemistry in capybaras (Hydrochoerus hydrochaeris) of human-modified landscapes and natural landscapes. Thesis submitted to the Postgraduate Program in Experimental Epidemiology Applied to Zoonoses of the School of Veterinary Medicine and Animal Science of the University of São Paulo to obtain the Doctor’s degree in Sciences.. Date: _____/_____/_____ Committee Members. Prof. ___________________________________________________________________________ Institution:________________________________ Decision:______________________________. Prof. ___________________________________________________________________________ Institution:________________________________ Decision:______________________________. Prof. ___________________________________________________________________________ Institution:________________________________ Decision:______________________________. Prof. ___________________________________________________________________________ Institution:________________________________ Decision:______________________________. Prof. ___________________________________________________________________________ Institution:________________________________ Decision:______________________________.

(7) DEDICATION. I dedicate this work to my parents, Cristina and Renato and to my brothers Diogo and Renan, for the 11504 days of support and unconditional love. Thank you for being my references..

(8) ACKNOWLEDGMENTS This study represents part of the results of a larger work. The result of countless fieldworks, hundreds of sampled capybaras and thousands of kilometers traveled. I am immensely grateful to everyone who took part in this common effort. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. First of all, I would like to thank Professor Marcelo Bahia Labruna, who received me in his laboratory, trusted my potential even when I doubted myself and to whom I owe much of what I have built in my academic career so far. From scientific initiation to the end of the doctorate (and maybe beyond). To my (co)advisor who ended up becoming a great friend, Hermes Ribeiro Luz. Thank you for the countless help and conversations, in good and bad times. Thank you for all the knowledge transmitted. Your company was one of the reasons why I came to the end of this journey. I also have enormous gratitude for my friends and professional colleagues Daniel Magalhães “Magras” Lima and Vinícius “Pôhnei” Dayoub, whom have been with me since the beginning of this work, both in my personal and professional life. I would also like to thank the professors and also friends Ricardo Dias and Fábio Gregori, who always kept their door open and was always extremely available for my (countless) doubts in the execution of my analyzes. Thank you for helping with my academic formation. I was lucky to work several times with excellent professionals and researchers, even in extremely exhausting field situations. Diego, Bira, Xico, Matias, Vanessa, Richard and Daniel. I am very grateful that my career has crossed with yours. Many times I felt honored to be part of the same team..

(9) My good friends: André “Xena” Storti Martins, Felipe “Joca” Juscele, Matheus “Fuleco” Cavalini. Thank you for more than ten years of friendship. You are an important part of my life. Dom Walter and Bebeth, thank you very much for your endless patience and the wonderful family lunches and meetings at the weekends for the past two years. To a recent friend, with whom, in the few times we met, I invested several hours of good conversations about research, science, academicism and future opportunities. Juan Diaz Ricaurte, my friend, thank you for contributing on the beginning of my journey in Science. To all the laboratory colleagues, who have already graduated or are still here, as well as the technicians, Pedro, Renatinho e Márcio. Thank you for being part of an always pleasant and very good-humored day at VPS. Danival and Vanessa, I owe you a lot of gratitude for always, very promptly, solving any problems and doubts that might arise. All field work was carried out outside the city of São Paulo, which was only made possible by the competence and professionalism of the transport personnel. Fábio, Flávio, Cidão, Mazza, João, Ivan, Muma and Josué. Thank you for all your help over the past four years and for the company in the thousands of kilometers traveled. Field sampling were often made possible thanks to the tireless help of the teams in each location. I would like to thank all the teachers, technicians, professionals, interns and students who showed constant concern for the work to be carried out. Of course, I could not fail to thank all the capybaras who, involuntarily, were an indispensable part of this work. Finally, the most important pillars of my life. To whom I am and I will be forever grateful. Mom, dad, I love you unconditionally. Thank you for absolutely everything you've done for me. Affection, support, encouragement, confidence, studies. I owe all my achievements to the great work you did..

(10) My grandmothers, Zelda and Osmilda, who, unfortunately, are no longer with us, but from whom I keep only affection and good memories. Thank you for being part of my personal formation. Di, thanks for being there for me whenever I needed it. Physical distance has never been an issue for our friendship and fellowship. Thank you for the conversations, for listening and for helping with my daily life. Renan, my brother, thanks for being there, even for financial help whenever I needed it. Thank you for being such a companion and friend for the past thirty years. We have fought a lot in this life, but we always remain united. Camila, my life partner. I'm sure that without you, your listening, your support and the endless patience I wouldn't have made this far. Thanks for everything. You have a direct participation in this achievement..

(11) “Life is short and potential studies infinite. We have a much better chance of accomplishing something significant when we follow our passionate interests and work in areas of deepest personal meaning” – Stephen Jay Gould (1941 – 2002).

(12) RESUMO BENATTI, H. R. Comparação de padrões morfométricos e bioquímica do sangue em capivaras (Hydrochoerus hydrochaeris) de paisagens modificadas pelo homem e paisagens naturais. 2020. 90 f. Tese (Doutorado em Ciências) – Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, 2020. A capivara (Hydrochoerus hydrochaeris) é o maior roedor do mundo, podendo atingir, até 100 kg, com o peso médio de indivíduos adultos de 50 kg. No sudeste brasileiro a capivara tem papel fundamental na manutenção da Febre Maculosa Brasileira (FMB), uma vez que funciona como hospedeiro amplificador para a bactéria Rickettsia rickettsii, agente causador da doença. Dentre as características necessárias para amplificação do agente, alta prolificidade e geração de novos indivíduos suscetíveis à rickettsemia são essenciais no cenário epidemiológico da FMB. Muitas paisagens modificadas pelo homem no sudeste do Brasil vivenciam expansão horizontal e vertical das populações de capivaras nas últimas décadas devido ao grande suprimento de alimentos, graças à expansão das monoculturas, como por exemplo, as canavieiras. Supôs-se, então, que as capivaras nas paisagens modificadas pelo homem (HMLs) estão aumentando suas reservas corporais, levandoas a um quadro de obesidade, quando comparadas às capivaras nas paisagens naturais (NLs) do bioma Pantanal do Brasil. Também se observou que a densidade populacional de capivaras em uma determinada área de ocupação é muito mais alta nas HMLs do que nas NLs, possivelmente por conta de um maior sucesso reprodutivo devido à oferta abundante de alimentos. Conjecturou-se, pois, que a obesidade dos animais em HMLs possa estar gerando distúrbios bioquímicos de natureza nutricional e metabólica. Esses distúrbios, somados a maiores capacidades reprodutivas, podem, portanto, aumentar as taxas de reposição de indivíduos, fazendo a manutenção da FMB no sudeste brasileiro. Objetivando responder a essas hipóteses, durante os anos 2015–2019, foram capturadas capivaras em sete HMLs no sudeste do Brasil, e em duas NLs do bioma Pantanal, todas com populações estabelecidas de capivaras. Foram realizadas coletas de sangue, mensuração de comprimento total, altura e circunferências de pescoço, tórax e abdômen, para comparar os resultados entre as populações, sendo as capivaras de NLs o grupo controle e as de HMLs o grupo experimental. Os resultados mostraram que os animais em HMLs eram mais pesados do que os animais nas NLs, e, apesar de mais pesados, eles não apresentavam medidas lineares maiores, excluindo qualquer tipo de interferência do tamanho nos valores de massa corporal dos indivíduos. Curiosamente, as capivaras de HMLs mostraram circunferências do pescoço e tórax maiores que aquelas registradas para capivaras em NLs. Além disso, o presente trabalho registrou um novo limite superior de peso para a espécie (105,2 kg). Ainda, os resultados encontrados nos exames de sangue demonstraram que, dos.

(13) onze fatores bioquímicos analisados, cinco (albumina, creatina quinase, colesterol, frutosamina e proteína total) foram significativamente diferentes entre as populações e dois (cálcio e aspartato aminotransferase) foram limítrofes. A análise de fatores bioquímicos direta ou indiretamente relacionados à obesidade comprova que as populações de capivaras de HMLs estão desenvolvendo, devido ao excesso de gordura, uma série de distúrbios bioquímicos de ordem metabólica e nutricional, que podem levar ao aumento das taxas de mortalidade nessas populações. Soma-se a isso o fato de que roedores expostos a dietas altamente energéticas tendem a exibir maior sucesso reprodutivo. Palavras-chave: capivara; paisagens modificadas pelo homem; paisagens naturais; padrão morfométrico; perfil bioquímico..

(14) ABSTRACT BENATTI, H. R. Comparison of morphometric patterns and blood biochemistry in capybaras (Hydrochoerus hydrochaeris) of human-modified landscapes and natural landscapes. 2020. 90 f. Thesis (Doctorate in Sciences) – School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, 2020.. The capybara (Hydrochoerus hydrochaeris) is the largest rodent in the world, reaching up to 100 kg, with an average adult weight of 50 kg. In southeastern Brazil, capybara occupy a fundamental role in maintaining Brazilian spotted fever (BSF), since it functions as an amplifying host for the bacterium Rickettsia rickettsii, the agent of the disease. Among the characteristics necessary for amplification of the agent, high prolificacy and generation of new individuals susceptible to rickettsemia are essential in the epidemiological scenario of BSF. Many human-modified landscapes (HMLs) in southeastern Brazil have experienced horizontal and vertical expansion of capybaras populations in recent decades due to the large supply of food, thanks to the expansion of crops, as for example, sugarcane. It was conjectured, then, that capybaras in HMLs are increasing their body reserves, leading them to a picture of obesity, when compared to capybaras in Natural Landscapes (NLs) of the Brazilian Pantanal biome. It was also observed that the population density of capybaras in a given occupation area is much higher in HMLs than in NLs, possibly due to greater reproductive success due to the abundant supply of food. It was conjectured, therefore, that the obesity of animals in HMLs may be generating biochemical disorders of nutritional and metabolic nature. These disorders, added to greater reproductive capacities, can therefore increase the replacement rates of individuals, maintaining the BSF in southeastern Brazil. To answer these hypotheses, during the years 2015–2019, capybaras were captured in seven HMLs in southeastern Brazil, and in two NLs of the Pantanal biome, all with established populations of capybaras. Blood collection, measurement of total length, height and circumferences of neck, thorax and abdomen were performed to compare the results between populations, with NLs capybaras being the control group and HMLs being the experimental group. The results showed that animals in HMLs were heavier than animals in NLs, and, despite being heavier, they did not present larger linear measurements, excluding any type of size interference in the individuals' body mass values. Interestingly, HMLs capybaras showed larger neck and chest circumferences than those recorded for NLs capybaras. In addition, the present work registered a new superior weight limit for the species (105.2 kg). The results.

(15) found in blood tests showed that, of the eleven biochemical factors analyzed, five (albumin, creatine kinase, cholesterol, fructosamine and total protein) were significantly different between populations and two (calcium and aspartate aminotransferase) were borderline. The analysis of biochemical factors directly or indirectly related to obesity proves that the capybara populations of HMLs are developing, due to excess fat, a series of biochemical disorders of metabolic and nutritional order, which can lead to increased mortality rates in these populations. In addition, rodents exposed to high-energy diets exhibit greater reproductive success. Keywords: capybara; human-modified landscapes; natural landscapes; morphometric pattern; biochemical profile..

(16) SUMMARY 1.. Background, hypotheses and objectives ...............................................................................17 1.1.. INTRODUCTION ......................................................................................................17. 1.2.. HYPOTHESES ...........................................................................................................24. 1.3.. OBJECTIVES .............................................................................................................26. 1.4.. REFERENCES ...........................................................................................................27. 1.5.. FIGURES LIST ..........................................................................................................32. 2. Human-modified landscapes sustain heavier population of free-living capybaras (Hydrochoerus hydrochaeris) in Brazil ..........................................................................................33 2.1.. ABSTRACT ................................................................................................................33. 2.2.. INTRODUCTION ......................................................................................................33. 2.3.. MATERIALS AND METHODS ...............................................................................35. 2.4.. RESULTS....................................................................................................................41. 2.5.. DISCUSSION..............................................................................................................49. 2.6.. REFERENCES ...........................................................................................................51. 2.7.. LIST OF ABBREVIATIONS ....................................................................................58. 2.8.. FIGURES LIST ..........................................................................................................59. 2.9.. TABLES LIST ............................................................................................................60. 3. Comparison of biochemical aspects related to obesity in free-ranging capybaras of Human-Modified Landscapes and Natural Landscapes .............................................................61. 4.. 3.1.. ABSTRACT ................................................................................................................61. 3.2.. INTRODUCTION ......................................................................................................61. 3.3.. MATERIALS AND METHODS ...............................................................................63. 3.4.. RESULTS AND DISCUSSION .................................................................................66. 3.5.. CONCLUSION ...........................................................................................................79. 3.6.. REFERENCES ...........................................................................................................80. 3.7.. LIST OF ABBREVIATIONS ....................................................................................86. 3.8.. FIGURES LIST ..........................................................................................................87. 3.9.. TABLES LIST ............................................................................................................88. Conclusions .............................................................................................................................89.

(17) 1. Background, hypotheses and objectives. 1.1. INTRODUCTION i.. Capybara (Hydrochoerus hydrochaeris). Capybara is a mammal native to Latin America and belongs to the order Rodentia, family Caviidae and genus Hydrochoerus. In this region, it has a wide distribution ranging from eastern Panama to Uruguay, including Brazil (ALHO et al, 1987). Only two species are known, Hydrochoerus isthmius (Colombia, Venezuela, Ecuador and Panama), and Hydrochoerus hydrochaeris, the later in all South American countries except for Chile. In Brazil, capybaras are widely distributed all over the country, except for its very scarce presence in the Caatinga biome (JIMÉNEZ, 1995; MOREIRA et al., 2013) (Fig. 1).. 17.

(18) Figure 1 – Distribution map of the genus Hydrochoerus spp. (Based on JIMÉNEZ, 1995; MOREIRA et al., 2013). 18.

(19) Capybaras are robust, semi-aquatic animals, being considered the largest extant rodent in the world, with adults reaching between 50 and 60 kg and at most 1.35 m in length (MOREIRA et al., 2013). They are strict herbivores with cecumcolic digestion, dependent on symbiosis with fermenting microorganisms (fungi, bacteria and protozoa);. therefore,. they. have. a. well. developed cecum (MOREIRA et al., 2013) (Fig. 2). Because of this, the capybara digestion process is very efficient, highlighting a high capacity to digest fibrous foods. Its digestive system, as a whole, is quite bulky, reaching an average capacity of 8.8L - 10L (OJASTI, 1973; BARROS. MORAES. et. al.,. 2002;. RODRIGUES et al., 2006). The diet basically consists of grazing grasses, also aquatic plants such as water hyacinths (BARRETO and QUINTANA, 2012). Interestingly, an adult capybara (40 kg) tends to consume about 3 to 5 kg of grass / day, and a young one (20 kg) consumes approximately 2 kg (SILVA, 1986).. Figure 2 - Schematic drawing of the digestive tract of capybaras. Adapted from Moreira et al (2013).. In natural situations, as occurs in the Brazilian Pantanal, during the water season and high food supply, the capybara selects the food and ingests smaller quantities, while in the dry season the selection is lower, but the intake is higher (HUME, 1989 ). In the State of São Paulo, where capybaras are close to sugarcane monocultures, this behavior of food selection can be reduced, since the amount of energy from the pasture is the main factor when capybaras choose what to eat (CORRIALE et al., 2011), and the supply of sugarcane is constant throughout the year (LORA et al., 2006). The capybara has a gestation period of 147-156 days (150 on average), yielding litters of 4 to 8 individuals. Sexual maturity is influenced by the climate, availability of resources 19.

(20) and lifestyle (OJASTI, 1973). According to Zara (1973), captive animals reach maturity at 15 months old, while López-Barbella (1984) states that wildlife animals reach the same status between 6 and 12 months old. In the wild, females start their reproductive life before males, when they reach body weight between 30 and 40 kg (OJASTI, 1973), which happens between 1.5 and 2 years. This condition can represent a problem in areas with strong anthropic action, where the food supply (e.g., crops) is vast and this weight can be reached before the age of 18 months; therefore, there is a possibility that the reproductive life of capybaras in these areas may begin earlier, increasing reproductive success (SHANER et al., 2018), and thus, increasing the size of the groups. In addition, males and females, weighing over 50 kg, have a higher reproductive performance (SILVA, 1986). ii.. Aspects of group formation and occupation of areas. Capybaras are social animals that form their groups close to water collections - rivers, lakes, flooded regions - because their sweat glands are not well developed (HERRERA, 2013); therefore, they need water bodies to regulate body temperature (homeothermy). In addition to thermal regulation, water bodies are a vital resource for capybara, not only for hydration, but also to escape from predators, mating and consumption of aquatic plant species (MACDONALD, 1981). Capybara live in groups composed by individuals of both sexes and all ages, with a varying number of individuals, from 5 to 100 per group, the latter being an atypical situation, outside the natural standards. Most socially stable groups do not reach more than 30 individuals (HERRERA et al., 2011). The size of the group is directly related to the reproductive success of the population (HERRERA and MACDONALD, 1989); however, in higher densities of larger societies this relationship is lost, since, possibly, the ideal size of the group has been exceeded (SALAS, 1999). iii.. Habitat loss, emergence and reemergence of diseases. The human needs to use land for food production causes the environment to be constantly modified, rapidly reducing natural areas and increasing areas of monoculture or 20.

(21) pasture. This sudden change in the environment causes a massive decrease in native fauna. In the most optimistic speculations, from 1970 until now, the populations of mammals, birds, reptiles, amphibians and fish fell by almost 30% (LOH, 2008). In Brazil, the destruction of native forests for the implantation of monocultures and pastures is a historical process, which took place in the country over the centuries (FAUSTO, 1994). In southeastern Brazil, one of the focus regions of the present study, the expansion of agriculture fields has caused a decrease in native fauna habitat areas (GHELER-COSTA et al. 2012) providing, however, an alternative food source of high energy for capybaras (BOVO et al. 2016). The advance of sugarcane crops caused a decrease in the habitat areas of native fauna. Along with these conditions, in the last decades, the State of São Paulo has been experiencing both horizontal and vertical expansion of capybaras populations. In the first case, capybaras started to occupy many areas where they did not exist before; in the second case, population densities have increased significantly in places of already established populations (VERDADE and FERRAZ, 2006; FERRAZ et al., 2007). It is known that changes in biodiversity, regardless of the biome, have the potential to affect the risk of exposure to diseases in plants and animals, including humans. Every infectious disease includes at least one pathogen and a host, and in the case of vector-borne diseases, there is one more species involved (KEESING, et al., 2006). According to Keesing et al. (2006) the loss of biodiversity can affect the transmission of infectious diseases by changing: (i) the abundance of the host or vector; (ii) the behavior of the host, the vector or the parasite; (iii) the environmental conditions for the host or vector. In some cases, a combination of more than one factor. Several lines of study demonstrated that the loss or reduction of biodiversity tends to increase the transmission of pathogens and the emergence or reemergence of diseases. This pattern has occurred in several ecosystems, with different pathogens, hosts and vectors. Several studies confirmed the theory of the correlation between environmental changes and the reduction of biodiversity and disease transmission: West Nile fever (EZENWA et al., 2006; SWADDLE and STAVROS, 2008; ALLAN et al., 2009); hantavirus (DIZNEY et al., 2009; CLAY et al., 2009); Lyme disease (OSTFELD et al., 2006; LOGIUDICE et al., 2008; KEESING et al., 2009), among others. For Brazilian spotted fever (BSF), Polo et al. (2015) 21.

(22) demonstrated that the increase and expansion of the sugarcane monoculture was directly related to the territorial expansion of human cases of the disease. iv.. Capybaras and the Brazilian spotted fever. Brazilian spotted fever, caused by the bacterium Rickettsia rickettsii, is the most severe and most prevalent tick-borne disease affecting humans in Brazil (LABRUNA, 2009). From 2001 to 2018, 978 cases of BSF were confirmed in the state of São Paulo, with a 50% lethality rate (LUZ et al. 2019). The more severe clinical picture is often due to failures in the initial diagnosis (DE LEMOS et al., 2001). In the southeastern region of Brazil, R. rickettsii is transmitted mainly by the tick Amblyomma sculptum, and by Amblyomma aureolatum in a few areas with different epidemiological conditions. In the state of São Paulo, A. aureolatum is the main vector in the metropolitan region of São Paulo, whereas A. sculptum is the main vector in degraded areas of the countryside of the state (GUEDES et al., 2005; PINTER and LABRUNA, 2006; LABRUNA, 2009; LUZ et al. 2019). While R. rickettsii in maintained in tick populations through transovarial and transstadial passages, it is known that the infection by R. rickettsii has some deleterious effect on ticks. Therefore, the R. rickettsii-infection rates tend to drop over consecutive tick generations, since the mortality of infected ticks is greater than in uninfected ticks (BURGDORFER, 1988; LABRUNA et al., 2011). Accordingly, the successful maintenance of R. rickettsii in a tick population depends on the participation of a vertebrate amplifying host, which once primarily infected, will develop a transient bacteremia (rickettsemia) for a few days, when new cohorts of R. rickettsii-infected ticks are created (BURGDORFER, 1988). To be considered a competent amplifying host, the vertebrate must: (i) be abundant in areas endemic for the agent; (ii) be the main host for the vectors; (iii) be susceptible to infection by R. rickettsii; (iv) once infected, must develop ricketsemia for a period of time sufficient to transmit the agent to other ticks that may parasitize it; (v) be prolific, therefore,. 22.

(23) produce descendants susceptible to the infection (LABRUNA, 2009). The capybara fulfills all the attributes listed above. In southeastern Brazil, where there are the highest numbers of BSF cases in Brazil, the anthropogenic actions have provided to capybaras a favorable environment for the formation of large groups (often over 30 animals), as previously mentioned (VERDADE and FERRAZ, 2006). In addition, with the loss of their natural habitat, capybaras are increasingly approaching areas of human occupation (parks, university campuses, closed condominiums), contributing to the constant maintenance of BSF in these areas (LABRUNA, 2013). In addition, in a recent study, Polo et al. (2017) reported that the dynamics of population densities of capybaras and A. sculptum in anthropogenic areas in the countryside of southeastern Brazil have a direct relationship in the spread of BSF in these regions.. 23.

(24) 1.2. HYPOTHESES It is hypothesized that the abundant food supply for capybaras in HMLs may be generating obese animals with biochemical disorders of nutritional and metabolic nature due to excess weight. These disorders could therefore be increasing the replacement rates of individuals susceptible to R. rickettsii in the population. In addition, the disorderly increase in groups of capybaras is essential for the maintenance of A. sculptum in the environment, especially in areas endemic to BSF (LUZ et al. 2019). In order to analyze such conjectures, the following hypotheses were elaborated: (I) For BODY MASS / SIZE ratio H0: The BODY MASS / SIZE ratio of capybaras in HMLs does not show statistical difference with the same relation of capybaras in NLs. H1: The mass / size ratio of capybaras in HMLs exhibits statistical difference with the same ratio of capybaras in NLs. Animals in HMLs are expected to be no larger; however, to be heavier than capybaras in NLs.. (II) For serum biochemical profile 1. Liver and kidney profile H0: The serum biochemical profile for liver enzymes (AST and AKP) and urea of capybaras in HMLs does not show significant difference in relation to capybaras in NLs. In other words, the biochemical profile of capybaras from different areas does not show significant differences. H1: The serum biochemical profile for liver enzymes (AST and AKP) and urea of capybaras in HMLs shows a significant difference in relation to capybaras in NLs. In other words, the biochemical profile of capybaras in different areas shows a significant difference. 2. Protein (total protein and serum albumin) and energy (fructosamine) metabolism and serum electrolytes (phosphorous and calcium) H0: Capybaras present in HMLs do not show any difference in protein and energy metabolism when compared to capybaras in NLs; capybaras from both landscapes do not exhibit differences regarding serum electrolyte concentrations.. 24.

(25) H1: Capybaras present in HMLs exhibit differences in protein and energy metabolism when compared to capybaras in NLs; capybaras from both landscapes exhibit some difference regarding to serum electrolyte concentrations.. 25.

(26) 1.3. OBJECTIVES Therefore, the general objective of the present study was to analyze a possible difference in the data obtained from body mass, body measurements and biochemical profile of capybaras captured in the Brazilian Pantanal (NLs), which will be our control group, and from capybaras sampled in HMLs in the state of São Paulo. Specific objectives: (I) To measure the total length, height and circumferences of the neck, thorax and abdomen of capybaras among HMLs and NLs; to determine body mass indexes of capybaras from the two landscapes and to evaluate possible differences between them. (II) To evaluate the biochemical profile of capybaras from HMLs and NLs based on eleven biochemical variables directly or indirectly related to increases in body energy reserves; to compare variables between capybaras from the two landscapes and to evaluate possible differences between them.. 26.

(27) 1.4.REFERENCES. ALHO, C. J. R., CAMPOS, Z. D. S., & GONÇALVES, H. C. (1987). Ecologia de capivara (Hydrochaeris hydrochaeris, Rodentia) do Pantanal: I Habitats, densidades e tamanho de grupo. Revista Brasileira de Biologia, 47(1/2). ALLAN, B. F., LANGERHANS, R. B., RYBERG, W. A., LANDESMAN, W. J., GRIFFIN, N. W., KATZ, R. S., & CLARK, L. (2009). Ecological correlates of risk and incidence of West Nile virus in the United States. Oecologia, 158(4), 699-708. BARRETO, G. R., & QUINTANA, R. D. (2013). Foraging strategies and feeding habits of capybaras. In Capybara (pp. 83-96). Springer, New York, NY. BOVO, A. A. D. A., FERRAZ, K. M. P. M. D., VERDADE, L. M., & MOREIRA, J. R. (2016). Capybaras (Hydrochoerus hydrochaeris) in anthropogenic environments: challenges and conflicts. Biodiversity in agricultural landscapes of southeastern Brazil. BURGDORFER, W. (1988). Ecological and epidemiological considerations of Rocky Mountain spotted fever and scrub typhus. Biology of rickettsial diseases, 1, 33-50. CLAY, C. A., LEHMER, E. M., JEOR, S. S., & DEARING, M. D. (2009). Sin Nombre virus and rodent species diversity: a test of the dilution and amplification hypotheses. PloS one, 4(7). CORRIALE, M. J., ARIAS, S. M., & QUINTANA, R. D. (2011). Forage quality of plant species consumed by capybaras (Hydrochoerus hydrochaeris) in the Paraná River Delta, Argentina. Rangeland Ecology & Management, 64(3), 257-263. DE BARROS MORAES, P. T., PACHECO, M. R., DE SOUZA, W. M., DA SILVA, R. A., NETO, P. B. S., DE FIGUEIREDO BARRETO, C. S., & RIBEIRO, A. A. C. M. (2002). Morphological aspects of the capybara stomach (Hydrochaeris hydrochaeris): gross and microscopic structure. Anatomia, histologia, embryologia, 31(6), 362-366.. 27.

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(29) HERRERA, E. A. (2013). Capybara social behavior and use of space: patterns and processes. In Capybara (pp. 195-207). Springer, New York, NY. HERRERA, E. A., & MACDONALD, D. W. (1989). Resource utilization and territoriality in group-living capybaras (Hydrochoerus hydrochaeris). The Journal of Animal Ecology, 667-679. HERRERA, E. A., SALAS, V., CONGDON, E. R., CORRIALE, M. J., & TANGMARTÍNEZ, Z. (2011). Capybara social structure and dispersal patterns: variations on a theme. Journal of Mammalogy, 92(1), 12-20. HUME,. I.. D.. (1989).. Optimal. digestive. strategies. in. mammalian. herbivores. Physiological Zoology, 62(6), 1145-1163. JIMÉNEZ, E. (1995). El capibara (Hydrochoerus hydrochaerus): estado actual de su producción. FAO, Roma (Italia). KEESING, F., et al (2009). Hosts as ecological traps for the vector of Lyme disease. Proceedings of the Royal Society B: Biological Sciences, 276(1675), 3911-3919. KEESING, F., HOLT, R. D., & OSTFELD, R. S. (2006). Effects of species diversity on disease risk. Ecology letters, 9(4), 485-498. LABRUNA, M. B. (2009). Ecology of rickettsia in South America. Ann NY Acad Sci, 1166(1), 156-166. LABRUNA, M. B. (2013). Brazilian spotted fever: the role of capybaras. In Capybara (pp. 371-383). Springer, New York, NY. LABRUNA, M. B. et al (2011). Experimental infection of Amblyomma aureolatum ticks with Rickettsia rickettsii. Emerging infectious diseases, 17(5), 829. LOGIUDICE, K., DUERR, S. T., NEWHOUSE, M. J., SCHMIDT, K. A., KILLILEA, M. E., & OSTFELD, R. S. (2008). Impact of host community composition on Lyme disease risk. Ecology, 89(10), 2841-2849.. 29.

(30) LOH, J. (2008). 2010 and Beyond. Rising to the Biodiversity Challenge. LÓPEZ-BARBELA, S. (1984). Una contribuición al conocimiento de la reproducción del chigüire. Informe Anual del IPA, Maracay, 109-117. LORA, B. A., MONTEIRO, M. B., ASSUNÇÃO, V., & FRIGERIO, R. (2006). Levantamento Georreferenciado da Expansão da Cultura de Cana-De-Açúcar no Estado de São Paulo (Georeferenced Assessment Of Sugarcane Culture Expansion in São Paulo State). São Paulo, December. LUZ, H. R., et al (2019). Epidemiology of capybara-associated Brazilian spotted fever. PLoS neglected tropical diseases, 13(9), e0007734. MACDONALD, D. W. (1981). Dwindling resources and the social behaviour of capybaras, (Hydrochoerus hydrochaeris)(Mammalia). Journal of Zoology, 194(3), 371391. MOREIRA, J. R., FERRAZ, K. M. P., HERRERA, E. A., & MACDONALD, D. W. (Eds.). (2013). Capybara: biology, use and conservation of an exceptional neotropical species. Springer Science & Business Media. OJASTI, J. (1973). Estudio biológico del chigüire o capibara (pp. 1-271). Caracas: Fondo Nacional de Investigaciones Agropecuarias. OSTFELD, R. S., CANHAM, C. D., OGGENFUSS, K., WINCHCOMBE, R. J., & KEESING, F. (2006). Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS biology, 4(6). PINTER, A., & LABRUNA, M. B. (2006). Isolation of Rickettsia rickettsii and Rickettsia bellii in cell culture from the tick Amblyomma aureolatum in Brazil. Annals of the New York Academy of Sciences, 1078(1), 523-529. POLO, G., LABRUNA, M. B., & FERREIRA, F. (2015). Satellite hyperspectral imagery to support tick-borne infectious diseases surveillance. PLoS One, 10(11).. 30.

(31) POLO, G., ACOSTA, C. M., LABRUNA, M. B., & FERREIRA, F. (2017). Transmission dynamics and control of Rickettsia rickettsii in populations of Hydrochoerus hydrochaeris and Amblyomma sculptum. PLoS neglected tropical diseases, 11(6), e0005613. RODRIGUES, S. S., FONSECA, C. C. F. C. C., FONSECA, C. C., DE PAULA, T. A. R., & PEIXOTO, J. V. (2006). Aspectos biométricos corporais e do intestino delgado da capivara. Hydrochoerus. hydrochaeris. Linnaeus,. 1766. (Mammalia,. Rodentia,. Hydrochaeridae). Biotemas, 19(3), 79-86. SALAS, V. (1999). Social organisation of capybaras in the Venezuelan Llanos (Doctoral dissertation, University of Cambridge). SHANER, P. J. L., YU, A. Y., LI, S. H., & HOU, C. H. (2018). The effects of food and parasitism on reproductive performance of a wild rodent. Ecology and evolution, 8(8), 4162-4172. SILVA, L.F.W. (1986) Criação de capivaras em cativeiro. São Paulo: Nobel, 69p. SWADDLE, J. P., & CALOS, S. E. (2008). Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect. PloS one, 3(6). VERDADE, L. M., & FERRAZ, K. M. P. M. B. (2006). Capybaras in an anthropogenic habitat in southeastern Brazil. Brazilian Journal of Biology, 66(1B), 371-378. VUCETICH, M. G., VIEYTES, E. C., PÉREZ, M. E., & CARLINI, A. A. (2010). 13 The rodents from La Cantera and the early evolution of caviomorphs in South America. The paleontology of Gran Barranca: evolution and environmental change through the Middle Cenozoic of Patagonia, 193. ZARA, J. L. (1973). Breeding and husbandry of AL‐capybara Hydrochoerus hydrochaeris at Evansville Zoo. International Zoo Yearbook, 13(1), 137-139.. 31.

(32) 1.5. FIGURES LIST Figure 1 – Distribution map of the genus Hydrochoerus spp. (Based on JIMÉNEZ, 1995; MOREIRA et al., 2013). (p. 18) Figure 2 - Schematic drawing of the digestive tract of capybaras. Adapted from Moreira et al (2013). (p. 19). 32.

(33) 2. Human-modified landscapes sustain heavier population of free-living capybaras (Hydrochoerus hydrochaeris) in Brazil 2.1.ABSTRACT The capybara (Hydrochoerus hydrochaeris) is the largest extant rodent in the world and, according to the literature, adults can reach between 50 and 60kg. Many humanmodified landscapes in southeastern Brazil have experienced horizontal and vertical expansion of capybaras populations in recent decades due to the large supply of food. It is conjectured that there is an increase in the energy reserves of capybaras in the humanmodified landscapes when compared to capybaras in natural landscapes of the Pantanal biome of Brazil. During 2015–2019, we captured capybaras in seven human-modified landscapes in the state of São Paulo, southeastern Brazil, and in two natural landscapes of the Pantanal biome, all with established populations of capybaras. Our results showed that animals in human-modified landscapes (61.2 kg ± 16.1) were heavier than animals in natural landscapes (54.2 kg ± 11.2), moreover the body measures as total length and height of both groups were similar, excluding any kind of interference in the body mass values of individuals.. Interestingly,. capybaras. from. human-modified. landscapes. showed. circumferences of the neck and thoracic measurements (60.9 cm ± 7.1; 90.4 cm ± 9.3, respectively) above those recorded for capybaras in natural landscapes (55.9 cm ± 5.5; 86.5 cm ± 7.4, respectively), indicating a possible relationship with body mass gain obtained by these animals. We concluded that the capybaras of human-modified landscapes were heavier when compared to capybaras of natural landscapes, which live in areas with low anthropogenic action. These higher body weights in human-modified landscapes are due to the constant availability of highly energetic foods, for example: sugarcane, very common in the state of São Paulo. Moreover, unlike natural landscapes, in anthropized areas these animals have limited movement to these food sources without any concern for predators. All of these elements lead to an increase in energy reserves in capybaras. 2.2. INTRODUCTION The capybara (Hydrochoerus hydrochaeris) is the largest living rodent in the world, reaching 50-60 kg in average (MOREIRA et al. 2013), being able to live socially in groups 33.

(34) formed from 5 to 100 individuals per group, the latter being an atypical situation outside the natural standards. Around 30 individuals typically compose the most socially stable groups known (HERRERA et al. 2011). Capybaras are native to all South American countries (except for Chile), most intensely from northern Venezuela to the mouth of the la Plata River in Argentina (FRAILEY 1986, VUCETICH et al. 2010, MOREIRA et al. 2013). The presence of capybaras in west of Andes in Panama, Colombia and Venezuela is thought represented by another species, smaller than the H. hydrochaeris, Hydrochoerus isthmius (MOREIRA et al. 2013). In southeastern Brazil, the expansion of agriculture fields has caused a decrease in native fauna habitat areas (GHELER-COSTA et al. 2012) providing, however, an alternative food source of high energy for capybaras (BOVO et al. 2016). Along with these conditions, the state of São Paulo has experienced a horizontal and vertical expansion of capybara populations in recent decades (VERDADE and FERRAZ 2006, FERRAZ et al. 2007, BOVO et al. 2016), and this highly nutritional agriculture crops are possibly enabling an increase in the energy reserves of these animals, thereby increasing their body conditions. Body condition is an important determinant of an animal's individual fitness and its implications are of great interest to ecologists, since animals with good body conditions and higher energetic reserves are more apt to survive and perpetuate the species (GREEN 2001). Besides, several authors have positively correlated higher energy body reserves with greater reproductive success (ATKINSON and RAMSAY 1995, DOBSON and MICHENER 1995, WAUTERS and DHONDT 1995). The horizontal and vertical expansion of capybara populations across humanmodified landscapes, made possible a better survival condition and the greater reproductive success is contributing to the increase of the encounter rates between humans and capybara populations, increasing conflicts and hazards regarding public safety and human health (LABRUNA 2013). The present study aimed to compare the body conditions of capybaras across humanmodified landscapes (HMLs) in the state of São Paulo and capybaras from natural landscapes (NLs) in the Pantanal biome of the states of Mato Grosso and Mato Grosso do Sul. For this 34.

(35) purpose, we analyzed linear measurements (body weight, height, length and perimeters) that are commonly used for rodents (SCHULTE-HOSTEDDE et al. 2001). While more accurate measurements regarding fat amount determination require the material to be destroyed and dissolved in solvents (DOBUSH et al. 1985), such lethal procedure was not possible in the present study. 2.3.MATERIALS AND METHODS Ethics approval and consent to participate This study was conducted under the approval of the Institutional Animal Care and Use Committee (IACUC) of the Faculty of Veterinary Medicine of the University of São Paulo (project number 5948070314), in accordance with the regulations/guidelines of the Brazilian National Council of Animal Experimentation (CONCEA). Field capture of capybaras were authorized by the Brazilian Ministry of the Environment (permit SISBIO Nos. 43259–6) and by the São Paulo Forestry Institute (Cotec permit 260108–000.409/2015). Study areas Captures of free-ranging capybaras were carried out during 2015-2019 in seven municipalities of the state of São Paulo (HMLs), and in two municipalities (NLs), one in the state of Mato Grosso and another one in the state of Mato Grosso do Sul (Table 1, Fig. 1). Capybara sampling was primarily performed for another study related to the epidemiology of Brazilian spotted fever - BSF (caused by the bacterium Rickettsia rickettsii), for which capybaras were consider to play a role as amplifying hosts of the bacterium to the capybara tick, Amblyomma sculptum, as described elsewhere (LUZ et al. 2019). We also included capybaras captured in two additional HMLs, Avaré and Tatuí, which were not included in the study of Luz et al. (2019). Among HMLs, sampled capybaras belonged to groups that were established adjacent to or within human settlements, such as farms, university campus, public or private parks, where capybaras had constant access to artificial pastures and crops. In NLs, sampled capybaras belonged to groups established in areas with no artificial pastures or crops, and with minimal anthropic changes during the last few decades. Detailed description of all sampled areas shown in Table S1.. 35.

(36) Table 1 – Location of capybara captures and sampling. Location. Municipality/State. Approximate Coordinate. Human Modified Landscapes (HMLs) University of São Paulo campus of. Piracicaba/SP. 22°43'05.1"S 47°36'39.6"W. Carioba sewage treatment station. Americana/SP. 22°42'35.7"S 47°20'24.5"W. Federal University of São Carlos. Araras/SP. 22°18'34.4"S 47°23'00.2"W. Private Company. Tatuí/SP. 23°22'42.4"S 47°55'01.0"W. University of São Paulo campus of. Pirassununga/SP. 21°56'52.4"S 47°27'13.6"W. Ribeirão Preto/SP. 21°10'03.9"S 47°51'30.7"W. Avaré/SP. 23°05'59.2"S 48°54'32.9"W. Piracicaba. campus of Araras. Pirassununga University of São Paulo campus of Ribeirão Preto Avaré State Park. Natural Landscapes (NLs) Pantanal of Poconé. Poconé/MT. 16°29'35.6"S 56°26'20.8"W. Pantanal of Nhecolândia. Corumbá/MS. 19°14'53.5"S 57°01'34.0"W. 36.

(37) Figure 1 - map representing each collection area. 37.

(38) Animal capture and containment Capybaras were captured by using 16 to 20 m² - corrals baited with sugar cane and green corn. Once closed in the corral, animals were physically restrained by a net catcher and anaesthetized with an intramuscular injection of a combination of ketamine (10 mg/kg) and xylazine (0.2 mg/kg). In Mato Grosso do Sul, corrals were not effective, thus capybaras were captured by anesthetic darting via a CO₂-injection rifle (Dan-Inject model JM Standard, Denmark) using the same chemicals described above (LUZ et al. 2019). In an attempt to interfere the minimum possible in animal health, all animals were always captured and handled in the early evening. Under anesthesia, animals were subjected to biometrical measures (described below) and identified with a subcutaneous microchip (Alflex model P/N 860005–001, Capalaba, Australia). After recovering from anesthesia, capybaras were released at the same capture site, as described elsewhere (LUZ et al. 2019). Biometrical measures For such analyses, only adult animals weighing >35.0 kg (MOREIRA et al. 2013) were measured, since body condition index should not be used to compare individuals of different ages, as it is supposed to reflect or to be validated by the amount of “absolute” or “percentage” energy tissue. This is because, at each stage of growth and development, the proportional or absolute amount of energy reserves can be expected to change with normal growth processes, even in an ideal environment (KOTIAHO 1999). For each sampled capybara, we measured the length, height and perimeter (neck, thorax and abdomen) of the body (in centimeters), as well as the body weight (kg), as commonly applied to biometric studies of rodents (PERGAMS and LAWLER 2009). The total length of the animals were measured from the end of the muzzle to the end of the last vertebra, and the height was measured from the highest point of the withers (with the capybara's paw stretched is measured from the tip of the largest finger to the upper margin of the scapula). The neck perimeter was measured at the angle of the mandible. The chest perimeter was measured at the height of the armpit and the circumference of the abdomen at 38.

(39) the umbilical line (Fig. 2). For all measures a polyester tape 150 cm long and 1 cm precision was used (Corrente Coats, Brazil). Weighing was done with the animal wrapped in a nylon net (weight 2.4 kg). The scale used was a digital dynamometer with a precision of 0.1 kg (Pesola model PCS0300, Hatton Rock, UK); it was attached to the net through a metal hook and then the net / animal set was suspended using a 1.5 m-aluminum bar.. a.. b.. Figure 2 - Representation of the measures taken from the capybaras. A. the linear measurements. B. the circumference measurements.. 39.

(40) Definition of Body Condition Index (BCI) Jakob et al. (1996) pointed out that the calculation of the body condition of animals is a common goal for several studies, in order to compare absolute size (or other measurement) with body mass; however, authors used several terminologies to indicate the same thing. In the present work, the adopted terminology was the "body condition index" (BCI), which was firstly proposed by Hepp et al. (1986). To our knowledge, information on body condition index (BCI) for the evaluation of large rodents are absent in the literature. Therefore, ratios previously applied to small rodents were extrapolated for capybaras, as follows: I.. BM / TL: Body mass (BM) divided by total length (TL) (LUNN and BOYD 1993, HUOT et al. 1995).. II.. BM / TL²: Body mass (BM) divided by the square of the total length (TL²) (TIERNEY et al. 2001, BERCOVITCH et al. 2003).. III.. BM / TL³: Body mass (BM) divided by the cube of the total length (TL³) (HUOT et al. 1995).. IV.. resBM / TL²: Residual of linear regression of body mass (resBM) divided by the square of total length (TL²) (CAVALLINI 1996).. V.. resBM / TL³: Residual of the linear regression of the body mass (resBM) divided by the cube of the total length (TL³) (TELLA et al. 1997, MCELROY et al. 2007).. Statistical analysis Data were evaluated using descriptive statistics, using violin-type density graphs and statistical summaries describing the groups through means and standard deviations for group comparison (HMLs versus NLs).. 40.

(41) Differences between capybaras from HMLs and NLs were assessed using the Student's t-test for parametric distributions or non-parametric Wilcoxon test. Normality was verified by the Shapiro-Wilk test and for all analyzes 5% was used as significance level. For statistical analysis, by standardization, only the most recent recaptures were included in the calculations. All analyzes were performed using R software (R Core Team, 2017, Vienna, Austria). Fat amount estimative An assumption of fat amount was estimated by calculating the residual index, which is the regressed body mass over body size. The residual index was calculated after data were appropriately transformed to meet regression assumptions. The residual distance from the point of the individual to the regression curve works as an estimate of the body condition, i.e. the distance from the point to the curve can be a good estimate of the extra mass accumulation, in this case, the fat (GOULD 1975). 2.4. RESULTS A total of 218 adult capybaras were sampled, 174 in HMLs and 44 in NLs (Table 2). Among these, 52 were recaptures. A total of 134 capybaras were analyzed in HMLs, and 32 in NLs. These capybaras were represented by 127 females and 39 males (Table 2).. 41.

(42) Table 2 – Number of adult capybaras sampled by locality of human-modified landscapes (HMLs) and natural landscapes (NLs) in Brazil Groups. Municipality. Number of adult capybaras Total. Recaptures. sampled HMLs. NLs. Included in the study Males. Females Total. Piracicaba. 38. 13. 3. 22. 25. Americana. 12. 2. 5. 5. 10. Araras. 17. 2. 1. 14. 15. Tatuí. 14. 0. 3. 11. 14. Pirassununga. 66. 13. 14. 39. 53. Ribeirão Preto. 22. 10. 4. 8. 12. Avaré. 5. 0. 1. 4. 5. TOTAL. 174. 40. 31. 103. 134. Poconé. 20. 10. 4. 6. 10. Corumbá. 24. 2. 4. 18. 22. TOTAL. 44. 12. 8. 24. 32. HMLs – Human-modified landscapes; NLs – Natural landscapes. Biometrics and weighing We recorded a weight range in adult capybaras of 35 - 105.2 kg, with three female capybaras, weighing 105.2, 104.8, and 100.6 kg were the overall heaviest animals, all captured in the HML, in Pirassununga municipality. Within the same experimental groups (HML or NL), there was no difference between weights and measures of male and female capybaras.. 42.

(43) The weight of adult capybaras of HMLs was, on average, 7 kg higher than the weight of animals from NLs (p = 0.005), with no significant differences in height and total length to explain this difference (Fig. 3 and 4; Table 3).. Figure 3 - graphic representation of the weight distribution in individuals according to the capture area. 43.

(44) Figure 4 - graphic representation of the measurement’s distribution of individuals according to the capture area. 44.

(45) Table 3 – comparison of biometric parameters between capybaras from humanmodified landscapes (HMLs) state and natural landscapes (NLs). Measurement. Region. Mean (SD). Height. HMLs. 55.9 (4.3). 57 (5.9). NLs. 56.1 (3.9). 56.8 (5.1). 127.3 (10.3). 129.2 (13.6). 126.4 (8.7). 126.5 (13.1). 98.7 (10.7). 99.5 (11.8). 97.6 (10.3). 100.2 (15.5). Total Length. HMLs NLs. Abdominal circumference HMLs NLs Neck circumference. Thoracic circumference. Weight. Median (IQR) P-Value 0.8. 0.69. 0.6578. HMLs. 60.9 (7.1). 60.8 (6.8) 0.000966. NLs. 55.9 (5.5). 57.2 (8.5). HMLs. 90.4 (9.3). 91.5 (11.6). NLs. 86.5 (7.4). 87.5 (10.1). HMLs. 61.2 (16.1). 62.7 (25.8). NLs. 54.2 (11.2). 55.7 (18.4). 0.049. 0.005. SD: Standard deviation.; IQR: Interquartile range; HMLs – Human-modified landscapes; NLs – Natural landscapes. By performing weight regression as a function of total length, height and gender, it was found that only total length explains a significant portion of weight variance. Thus, the residue of weight regression as a function of total length functions as an approximation of the amount of fat deposited an important variable in animal weight composition (Fig. 5). Note: the r² of both models is about the same 75%.. 45.

(46) Figure 5 - graphic representation of the distribution of weight in relation with the total length of capybaras according to the region. Regarding the circumference measurements, we observed statistical differences in two of the three measurements: neck and chest. Abdominal circumference did not differ between populations (Table 3). Definition of Body Condition Index (BCI) By comparing all the BCI, there was a statistical difference between the two groups, and the BCI of animals across HMLs was significantly higher than the group of capybaras resident in NLs (Table 4). Regardless of the formula used to calculate the body condition index, there was always differences between the two groups, and animals from HMLs had higher body index (Fig. 6).. 46.

(47) Table 4 - Body Condition Index average values of capybaras from human-modified landscapes (HMLs) and natural landscapes (NLs) Formula. Region. Mean (SD). P-value. MC/CT. HMLs. 0.4928 (0.0965). 0.005. NLs. 0.4410 (0,0656). HMLs. 0,0038 (0.0005). NLs. 0.0035 (0,0004). MC/CT². MC/CT³. Residue. HMLs. 3.03E+5 (3.64E+3). NLs. 2.75E+5 (2.62E+3). HMLs NLs. resMC/CT². resMC/CT³. HMLs. 1.37 (8.01). <0.001. <0.001. -4.74 (4.89) 8.75E+5 (0.00048). NLs. -2.9E+11 (0.00031). HMLs. 7.18E+1 (3.79E+3). NLs. <0.001. <0.001. <0.001. -2.28E+3 (2.57E+3). BM / TL: Body mass (BM) divided by total length (TL); BM / TL²: Body mass (BM) divided by the square of the total length (TL²); BM / TL³: Body mass (BM) divided by the cube of the total length (TL³); resBM / TL²: Residual of linear regression of body mass (resBM) divided by the square of total length (TL²); resBM / TL³: Residual of the linear regression of the body mass (resBM) divided by the cube of the total length (TL³). 47.

(48) Figure 6 - graphic representation of the distribution of Body Condition Indexes according to the capture area. 48.

(49) 2.5. DISCUSSION It was observed that HML capybaras are heavier than NL capybaras, although the total length and height do not differ statistically. Previous work has recorded weights of these animals, but to our knowledge, none of them compares populations from different areas. Mones and Ojasti (1986) recorded in Llanos, Venezuela, a weight range in adults between 35 - 65 kg, while Alho (1986) recorded in the Brazilian Pantanal, capybaras of up to 70 kg. Interestingly, the sampling sites of Alho (1986) are in the same region as the present study, where we recorded in the Brazilian Pantanal (NLs), a 79.8 kg animal, almost 10 kg heavier than the old limit registered for the species in the local. Other authors record species boundaries without defining location, as is the case with MacDonald et al. (2007), in which he defines the weight range for adult capybaras between 35 - 66 kg with an average of 50 kg. Moreira et al. (2013) defines the weight range between 35 100kg for the species, also with an average of 50kg. Our work defines that H. hydrochaeris must have separate weight averages depending on the type of environment it occupies (HML or NL). In both cases, we obtained different values from those reported in the literature. For the HMLs we obtained a range of 35 - 105.2 kg, registering a new weight limit for the species, with an average of 61.2 kg. For NLs capybaras the weight range is 35 - 79.8 kg, with an average of 54.2 kg. The five body index showed differences between the sampled groups, revealing that capybaras in the HMLs had higher BCI than capybaras in the NLs; therefore, higher fat reserves. We can infer that the extra weight of animals from HMLs comes from excess fat, since most of the fat in a capybara is subcutaneous (BRESSAN et al. 2002). The measurements of the perimeters indicated higher fat deposits in animals in the HMLs. Even though Jakob et al. (1996) stated that results vary dramatically according to the BCI chosen to calculate and to analyze body condition, in the case of our work, this was not a problem, since the main idea was to show that there was a difference in weight and BCI between. 49.

(50) the two sampled groups (HMLs and NLs), and all of our BCI results showed that difference between the populations. Since body condition is treated as a measure of energy status, animals in better conditions for survival are expected to have higher energy reserves (usually fat) (SCHULTE-HOSTEDDE et al. 2001). Therefore, based in individual energy reserves, we can infer that capybaras from HMLs have better survival conditions than animals from NLs. Firstly, due to the vast supply of food offered by crops (e.g., sugarcane, corn) throughout the state of São Paulo (FERRAZ et al. 2007). Secondly, besides the presence of pumas (Puma concolor), a natural predator of capybaras in HMLs (ANGELIERI, et al. 2016), heavier animals are able to some extent avoid predation, despite having impaired locomotion (TROMBULAK 1989). In addition to the possible better survival conditions of capybaras in HMLs, it is known that both natural and sexual selection tend to favor larger and heavier individuals (SELK et al. 1988, BLANCKENHORN 2000). The obvious, although fundamental, generalization is that the greater the availability of limiting resources, the larger the population size (MOREIRA et al. 2013). A trait that responds to food availability, such as body mass, is likely to covary with fitness at the phenotypic level; i.e., individuals that have access to more food are heavier and reproduce more (SCHLUTER et al. 1991). There are studies with domestic cattle considering body condition and reproductive efficiency, the higher the BCI, the better the reproductive efficiency (PRYCE et al. 2001). This association stems from the fact that the corpus luteum might be directly activated by cholesterol, a progesterone precursor (ROCHE et al. 2007). There are also reports of relationship between blood fatty acids and prostaglandin production. The direct effect of positive energy balance (energy consumed minus energy required for maintenance) on luteinizing hormone secretion has been demonstrated in heifers for over 30 years (IMAKAWA et al. 1987). Therefore, there is a great possibility that capybaras in HMLs, due to access to abundant food supply, are reproducing on larger scales than the animals of NLs, thus forming larger groups. Population growth either horizontally or vertically has led to greater approximations between capybara and man. This approach in the HMLs of the state of São Paulo has been 50.

(51) routinely covered by the media (Gazeta de Piracicaba 2019, Jornal da USP 2019, Estadão 2019). It is not uncommon for humans and capybaras to live in the same environment, for example, university campus, luxury residential parks, municipal parks and, in some cases, even within the city, next to water collections (VERDADE and FERRAZ 2006, BOVO et al. 2016, ROCHA et al. 2017, PASSOS NUNES et al., 2019). Such proximity has brought certain losses with regard to public health and safety (LABRUNA 2013, ABRA et al. 2019, PASSOS NUNES et al. 2019). Among HMLs, capybaras are major hosts for the tick A. sculptum, the vector of R. rickettsii, the agent of Brazilian Spotted Fever (BSF) in the countryside of the state of São Paulo. BSF is the main and most lethal tick-borne disease of humans in Brazil (LABRUNA 2009). The clinical picture is severe and often due to failures in the initial diagnosis, of fatal course (DE LEMOS et al. 2001). From 2001 to 2018, over 978 cases of BSF were confirmed of which 489 had a fatal outcome, a 50% fatality rate (LUZ et al. 2019). CONCLUSION We concluded that capybaras of HMLs in the state of São Paulo are heavier, but not larger, when compared to capybaras of NLs in the Brazilian Pantanal, which reinforces the mass gain of animals in HMLs. Also, capybaras in HMLs had larger circumferences of the neck and chest, region where these animals commonly have subcutaneous fat accumulation. This increase in energetic reserves has enabled the spread of capybara populations in the HMLs, which might have brought several consequences regarding health and public safety, as well as deleterious consequences for capybaras themselves. 2.6. REFERENCES ALHO, C. J. R. (1986). Criação e manejo de capivaras em pequenas propriedades rurais. Área de Informação da Sede-Documentos (INFOTECA-E). ANGELIERI, C. C. S., ADAMS-HOSKING, C., & DE BARROS, K. M. P. M. (2016). Using species distribution models to predict potential landscape restoration effects on puma conservation. PLoS One, 11(1).. 51.

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